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Natural Selection Drives Chemical Resistance of Datura Stramonium

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Natural Selection Drives Chemical Resistance of Datura Stramonium Natural selection drives chemical resistance of Datura stramonium Adán Miranda-Pérez1, Guillermo Castillo1,2, Johnattan Hernández-Cumplido3, Pedro L. Valverde4, María Borbolla1, Laura L. Cruz1, Rosalinda Tapia-López1, Juan Fornoni1, César M. Flores-Ortiz5 and Juan Núñez-Farfán1 1 Laboratory of Ecological Genetics and Evolution, Department of Evolutionary Ecology, Institute for Ecology, Universidad Nacional Autónoma de México, Mexico City, México 2 Laboratorio Nacional de Análisis y Síntesis Ecológica, Escuela Nacional de Estudios Superiores, Universidad Nacional Autónoma de México, Campus Morelia, Michoacán, México 3 Department of Entomology, Rutgers University, P.E. Marucci Center, Chatsworth, NJ, United States 4 Department of Biology, Universidad Autónoma Metropolitana, Mexico City, México 5 UBIPRO, Facultad de Estudios Superiores Iztacala Universidad, Nacional Autónoma de México, Tlalnepantla, México ABSTRACT Plant resistance to herbivores involves physical and chemical plant traits that prevent or diminish damage by herbivores, and hence may promote coevolutionary arm-races between interacting species. Although Datura stramonium's concentration of tropane alkaloids is under selection by leaf beetles, it is not known whether chemical defense reduces seed predation by the specialist weevil, Trichobaris soror, and if it is evolving by natural selection. We measured infestation by T. soror as well as the concentration of the plants' two main tropane alkaloids in 278 D. stramonium plants belonging to 31 populations in central Mexico. We assessed whether the seed predator exerted preferences on the levels of both alkaloids and whether they affect plant fitness. Results show great variation across populations in the concentration of scopolamine and atropine in both leaves and seeds of plants of D. stramonium, as well as in the intensity of infestation and the proportion of infested fruits by T. soror. The concentration of scopolamine in seeds and leaves are negatively associated across populations. We found that scopolamine concentration increases plant fitness. Our major finding was the Submitted 7 January 2016 detection of a positive relationship between the population average concentrations of Accepted 14 March 2016 scopolamine with the selection differentials of scopolamine. Such spatial variation in Published 14 April 2016 the direction and intensity of selection on scopolamine may represent a coevolutionary Corresponding author selective mosaic. Our results support the view that variation in the concentration of Juan Núñez-Farfán, [email protected] scopolamine among-populations of D. stramonium in central Mexico is being driven, Academic editor in part, by selection exerted by T. soror, pointing an adaptive role of tropane alkaloids Marion Röder in this plant species. Additional Information and Declarations can be found on page 13 Subjects Ecology, Entomology, Evolutionary Studies, Plant Science DOI 10.7717/peerj.1898 Keywords Trichobaris soror, Datura stramonium, Natural selection, Plant resistance, Seed predation, Tropane alkaloids, Selection differential, Scopolamine, Atropine Copyright 2016 Miranda-Pérez et al. Distributed under INTRODUCTION Creative Commons CC-BY 4.0 The coevolutionary process involves reciprocal selection-adaptation between interacting OPEN ACCESS species through time (Dawkins & Krebs, 1979; Thompson, 1999; Thompson, 2005). This How to cite this article Miranda-Pérez et al. (2016), Natural selection drives chemical resistance of Datura stramonium. PeerJ 4:e1898; DOI 10.7717/peerj.1898 adaptation and counter-adaptation phenomenon could result in a coevolutionary arms race, a process of offense-defense (Dawkins & Krebs, 1979). A coevolutionary relationship between plants and herbivores may generate symmetrical or asymmetrical selective pressures between interacting species. These selective pressures may be different spatially and could produce a geographic structure of interactions (Forde, Thompson & Bohannan, 2004; Gomulkiewicz et al., 2002; Nuismer, Thompson & Gomulkiewicz, 2000; Thompson, 1999; Thompson, 2005). In some locations the interacting species exert reciprocal selection pressures to one another (coevolutionary hot spots), whereas in other locations reciprocal selection is highly asymmetric (coevolutionary cold spots) (Gomulkiewicz et al., 2002; Nuismer, Thompson & Gomulkiewicz, 2000; Thompson, 1999; Thompson, 2005). A coevolutionary arms race between herbivores and plants may be favored in specialized interactions as in the case of insects that detoxify specific compounds (Janzen, 1969; Janzen, 1973; Schoonhoven, Van Loon & Dicke, 2005). For instance, the aphid Macrosiphum albifrons is adapted to consume Lupinus angustifolius with a low content of alkaloids (Philippi et al., 2015); however, dietary specialist herbivore insects may also be adapted to tolerate secondary metabolites of their host plants without switching to other different host plants (Laukkanen et al., 2012). In Arabidopsis thaliana, the abundance of two aphid herbivore species is correlated to a genetic polymorphism of the plant's resistance locus. This polymorphism is under selection due to changes in population size of the two aphid species (Züst et al., 2012). Host-parasite systems, that exert reciprocal selection pressures, offer the opportunity to assess the asymmetry in selection pressures and the potential to produce adaptation (Greischar & Koskella, 2007). Local adaptation may produce population differentiation as a by-product of natural selection (Kawecki & Ebert, 2004). This process is well illustrated by the weevil Curculio camelliae (Coleoptera: Curculionidae) that parasitizes the fruits of Camellia japonica (Theaceae) (Iseki, Sasaki & Toju, 2011; Toju, 2007; Toju, 2009; Toju & Sota, 2006). The fruits of C. japonica are capsules with a thick pericarp, dehiscent, with three locules and one seed per cavity (Okamoto, 1988). Females of C. camelliae perforate the thick pericarp with its long rostrum, modified labial cavity in insects (Resh & Cardé, 2009), and oviposit on the seeds (Toju, 2007). A successful weevil infestation, or oviposition, depends on the phenotypic match between the rostrum length and pericarp thickness. These two traits that mediate the interaction vary geographically and are under selection (Toju, 2007; Toju, 2009; Toju & Sota, 2006). Some evidence, however, indicates that these phenotypic characteristics may also vary according to abiotic factors, i.e., the latitude (Iseki, Sasaki & Toju, 2011). Furthermore, infestation by the weevil C. camelliae increases at higher-altitude localities and its obligated host plant decreases its resistance (Toju, 2009). In the C. camelliae-C. japonica system, natural selection acts on pericarp thickness that is a physical barrier that prevents infestation by weevils (Toju, 2007; Toju, 2009; Toju & Sota, 2006). In the annual herb Datura stramonium, tropane alkaloids function either as resistance characters preventing foliar damage by herbivores and/or as phagostimulants to them (Castillo et al., 2013; Castillo et al., 2014; Shonle & Bergelson, 2000). Evidence shows that alkaloid concentration in D. stramonium varies across populations (Castillo et al., 2014) Miranda-Pérez et al. (2016), PeerJ, DOI 10.7717/peerj.1898 2/17 and that such differentiation in chemical defense could be adaptive (Castillo et al., 2015). In some populations, dietary specialist and generalist folivores select against atropine concentration, whereas scopolamine is positively selected selected by the dietary specialist folivore Lema daturaphila and by the generalist grasshopper Sphenarium purpurascens (Castillo et al., 2014). Fruits of D. stramonium are parasitized by Trichobaris soror (Coleoptera: Curculionidae) that reduces plant fitness by consuming the seeds (Cabrales-Vargas, 1991; Cruz, 2009; De-la-Mora, Piñero & Núñez-Farfán, 2015). However, to what extent alkaloids of D. stramonium could affect infestation by the seed predator is not known. Here, we analyzed the relationship between tropane alkaloids produced by D. stramonium and infestation by the specialized seed predator T. soror across multiple populations in central Mexico. We aimed to determine whether D. stramonium's tropane alkaloids prevent infestation by T. soror. Specifically, we addressed the following questions: 1. Are alkaloids resistance characters that prevent/reduce infestation by weevils; 2. Do seed predators exert natural selection upon plant's alkaloids concentration; and 3. Do variation of both alkaloid concentration and infestation by weevils across populations is correlated to the localities' environmental conditions? (v. gr., Toju, 2009). MATERIALS AND METHODS Study system The weevil Trichobaris soror (Coleoptera: Curculionidae) is intimately associated to the life cycle of D. stramonium (Bello-Bedoy, Cruz & Núñez-Farfán, 2011a; Borbolla, 2015; Cabrales-Vargas, 1991). Trichobaris soror is distributed mainly in central Mexico (Barber, 1935; De-la-Mora, Piñero & Núñez-Farfán, 2015); adult weevils feed on leaves, calyx and floral tissues of D. stramonium. After mating, females oviposit at the base of developing fruits. Their larvae feed exclusively on immature seeds inside the developing fruit where they build tunnels with their own feces. Larvae pupate in the fruit and sometimes are parasitized by wasps. The weevils hibernate inside the fruit of D. stramonium until the next rainy season (Bello-Bedoy, Cruz & Núñez-Farfán, 2011a; Borbolla, 2015; Cabrales-Vargas, 1991). Besides the seed predator, D. stramonium
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